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      Behavioral changes and dendritic remodeling of hippocampal neurons in adolescent alcohol-treated rats

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          Abstract

          Objective: Earlier, we and others have reported that alcohol exposure in adolescent rat impaired performance of a spatial memory task in the Morris water maze. The goal of the present study was to investigate the effects of acute adolescent alcohol treatment on the hippocampus-dependent (contextual fear conditioning) and hippocampus-independent (cued fear) memories. The study also looked at the structural changes in anterior CA1 hippocampal neurons in adolescent alcohol-treated rats.

          Methods: Adolescent female rats were administered with a single dose of alcohol (1.0, 1.5, or 2.0 g/kg) or vehicle either before training (pre-training) or after training (pre-testing). Experimental and control rats were trained in the fear conditioning paradigm, and 24 h later tested for both contextual fear conditioning as well as cued fear memory. Separate groups of rats were treated with either alcohol (2 g/kg) or vehicle and sacrificed 24 h later. Their brains were harvested and processed for rapid Golgi staining. Randomly selected CA1 pyramidal neurons were analyzed for dendritic branching and dendritic spine density.

          Results: Pre-training alcohol dose-dependently attenuated acquisition of hippocampus-dependent contextual fear conditioning but had no effect on the acquisition of amygdala-associated cued fear. When administered following training (pre-testing), alcohol did not alter either contextual conditioning or cued fear memory. Golgi stained CA1 pyramidal neurons in alcohol treated female rats had reduced basilar tree branching and less complex dendritic arborization.

          Conclusion: Alcohol specifically impaired hippocampal learning in adolescent rats but not amygdala-associated cued fear memory. Compared to vehicle-treated rats, CA1 hippocampal pyramidal neurons in alcohol-treated rats had less complex dendritic morphology. Together, these data suggest that adolescent alcohol exposure produces changes in the neuronal organization of the hippocampus, and these changes may be related to impairments in hippocampus-dependent memory formation.

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          Most cited references47

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          Modality-specific retrograde amnesia of fear.

          Emotional responses such as fear are rapidly acquired through classical conditioning. This report examines the neural substrate underlying memory of acquired fear. Rats were classically conditioned to fear both tone and context through the use of aversive foot shocks. Lesions were made in the hippocampus either 1, 7, 14, or 28 days after training. Contextual fear was abolished in the rats that received lesions 1 day after fear conditioning. However, rats for which the interval between learning and hippocampal lesions was longer retained significant contextual fear memory. In the same animals, lesions did not affect fear response to the tone at any time. These results indicate that fear memory is not a single process and that the hippocampus may have a time-limited role in associative fear memories evoked by polymodal (contextual) but not unimodal (tone) sensory stimuli.
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            Effects of adolescent alcohol consumption on the brain and behaviour

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              Adolescent Brain Development and the Risk for Alcohol and Other Drug Problems

              Dynamic changes in neurochemistry, fiber architecture, and tissue composition occur in the adolescent brain. The course of these maturational processes is being charted with greater specificity, owing to advances in neuroimaging and indicate grey matter volume reductions and protracted development of white matter in regions known to support complex cognition and behavior. Though fronto-subcortical circuitry development is notable during adolescence, asynchronous maturation of prefrontal and limbic systems may render youth more vulnerable to risky behaviors such as substance use. Indeed, binge-pattern alcohol consumption and comorbid marijuana use are common among adolescents, and are associated with neural consequences. This review summarizes the unique characteristics of adolescent brain development, particularly aspects that predispose individuals to reward seeking and risky choices during this phase of life, and discusses the influence of substance use on neuromaturation. Together, findings in this arena underscore the importance of refined research and programming efforts in adolescent health and interventional needs.
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                Author and article information

                Contributors
                Journal
                Adv Drug Alcohol Res
                Adv Drug Alcohol Res
                Adv. Drug Alcohol Res.
                Advances in Drug and Alcohol Research
                Frontiers Media S.A.
                2674-0001
                24 July 2023
                2023
                : 3
                : 11158
                Affiliations
                [1] 1 Department of Psychology , The City College of New York , City University of New York , New York, NY, United States
                [2] 2 Department of Psychiatry and Behavioral Sciences , Albert Einstein College of Medicine , Bronx, NY, United States
                Author notes

                Edited by: Emmanuel Onaivi, William Paterson University, United States

                Reviewed by: Sonya Krishna Sobrian, Howard University, United States

                Douglas Matthews, University of Wisconsin–Eau Claire, United States

                *Correspondence: Ratna Sircar, rsircar@ 123456ccny.cuny.edu
                Article
                11158
                10.3389/adar.2023.11158
                10880782
                38389817
                0384f69d-35d5-4e5b-95e9-52ea987e91c7
                Copyright © 2023 Sircar.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 December 2022
                : 18 May 2023
                Funding
                Research was supported by NIH grant AA017359 (RS). This source of funding did not play any role in study design, data collection, analysis and interpretation, in writing the report, or in the decision to submit the article for publication. Some of the experiments were performed at the Feinstein Institute for Medical Research, Manhasset, NY.
                Categories
                Health Archive
                Original Research

                teenage drinking,alcohol blackout,contextual fear conditioning,dendritic branching,cued fear memory

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